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Disease states associated with telomerase deficiency appear earlier in mice with short telomeres
Open accessAbstract
Mice deficient for the mouse telomerase RNA (mTR-/-) and lacking telomerase activity can only be bred for approximately six generations due to decreased male and female fertility and to an increased embryonic lethality associated with a neural tube closure defect. Although late generation mTR-/- mice show defects in the hematopoietic system, they are viable to adulthood, only showing a decrease in viability in old age. To assess the contribution of genetic background to the effect of telomerase deficiency on viability, we generated mTR-/- mutants on a C57BL6 background, which showed shorter telomeres than the original mixed genetic background C57BL6/129Sv. Interestingly, these mice could be bred for only four generations and the survival of late generation mTR-/- mice decreased dramatically with age as compared with their wild-type counterparts. Fifty percent of the generation 4 mice die at only 5 months of age. This decreased viability with age in the late generation mice is coincident with telomere shortening, sterility, splenic atrophy, reduced proliferative capacity of B and T cells, abnormal hematology and atrophy of the small intestine. These results indicate that telomere shortening in mTR-/- mice leads to progressive loss of organismal viability.
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“However, the cyclin-dependent kinase inhibitor p21 has been shown to participate in the p53-dependent telomere checkpoint response in both human fibroblasts and in TERCÀ/À mice (66,76).”
From Telomeres and telomerase in cancer (2010) · cites this paper as [76]
In the citing paper
“Although it was initially clear that high-turnover tissues are particularly sensitive to telomere length85,101,112”
From The telomere syndromes (2012) · cites this paper as [112]
In the citing paper
“In particular, mice carrying a homozygous germline deletion of the telomerase RNA component gene (Terc−/−) exhibit critically short telomeres and a premature development of age-related pathologies from the second or third generation [8, 18–20, 51, 70, 72, 101, 103]”
From Senescence-related impairment of autophagy induces toxic intraneuronal amyloid-β accumulation in a mouse model of amyloid pathology (2023) · cites this paper as [51]
In the citing paper
“the generation and characterization of the telomerase knockout mouse model has been instrumental in demonstrating that short telomeres result in multiple organismal defects caused by defective tissue regeneration 57, 58, 59”
From The common biology of cancer and ageing (2007) · cites this paper as [59]
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Self-citationShort Telomeres, even in the Presence of Telomerase, Limit Tissue Renewal Capacity
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“Importantly, telomerase-deficient mice show worsening of phenotypes with increasing mouse generations owing to inherited progressively shorter telomeres, with the later generations showing severe phenotypes and premature death at pre-reproductive ages (Garcı́a-Cao et al., 2002; Herrera et al., 1999; Lee et al., 1998).”
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“These include immune senescence, loss and graying of hair, and impaired wound healing (Rudolph et al., 1999; Herrera et al., 1999, 2000).”
BackgroundMammalian telomeres and telomerase
Collins, K. (2000) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(00)00103-4 · Cited by 226
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Self-citationTelomere Maintenance Requires the RAD51D Recombination/Repair Protein
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Self-citationThe Rate of Increase of Short Telomeres Predicts Longevity in Mammals
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“In further support of this notion, both telomerase-deficient mice and human diseases due to mutations in telomerase components result in accelerated-aging phenotypes and decreased longevity due to premature depletion of stem cells and subsequent organ/tissue failure (Armanios et al., 2007; Blasco et al., 1997; Garcı́a…”
BackgroundSelf-citationMammalian Ku86 mediates chromosomal fusions and apoptosis caused by critically short telomeres
Espejel, S., Franco, S., Rodríguez, S., Bouffler, S. D., Cigudosa, J. C., & Blasco, M. A. (2002) · The EMBO Journal · doi:10.1093/emboj/21.9.2207 · Cited by 222
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Self-citationA ‘higher order’ of telomere regulation: telomere heterochromatin and telomeric RNAs
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“…in stem cell dysfunction, premature loss of tissue regeneration, and reduced life span, as shown in the context of telomerase-deficient mice (Blasco et al, 1997; Herrera et al, 1999; Rudolph et al, 1999; Gonzalez-Suarez et al, 2000; Collins and Mitchell, 2002; Blasco, 2005; Garcia-Cao et al, 2006).”
BackgroundSelf-citationTelomere Shortening Exposes Functions for the Mouse Werner and Bloom Syndrome Genes
Du, X., Shen, J., Kugan, N., Furth, E. E., Lombard, D. B., Cheung, C., Pak, S., Luo, G., Pignolo, R. J., DePinho, R. A., et al. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.19.8437-8446.2004 · Cited by 213
“However, crypt cells do apoptose in lategeneration telomerase mutants (17, 44).”
BackgroundResultCancer predisposition and hematopoietic failure in Rad50 S/S mice
Bender, C. F., Sikes, M. L., Sullivan, R., Huye, L. E., Le Beau, M. M., Roth, D. B., Mirzoeva, O. K., Oltz, E. M., & Petrini, J. H. J. (2002) · Genes & Development · doi:10.1101/gad.1007902 · Cited by 213
“In this regard, the Rad50 mice are similar to late-generation telomerase-deficient (mTR) mice, which experience telomere failure as a sequela to telomere shortening, and exhibit relatively selective depletion of hematopoietic and spermatogenic cells (Lee et al. 1998; Herrera et al. 1999).”
BackgroundInfluentialMechanisms of Aging and the Preventive Effects of Resveratrol on Age-Related Diseases
Pyo, I. S., Yun, S., Yoon, Y. E., Choi, J. W., & Lee, S. (2020) · Molecules · doi:10.3390/molecules25204649 · Cited by 221
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“Whether sufficient to lead to that particular outcome or not, telomere shortening has been clearly associated with chronological aging and, perhaps more interestingly, it has been found that telomere shortening is accelerated by psychological stress (Herrera et al. 1999; Blasco 2007; Parks et al. 2009; Zalli et al. 20…”
BackgroundRole of Telomerase in Normal and Cancer Cells
Meyerson, M. M. (2000) · Journal of Clinical Oncology · doi:10.1200/jco.2000.18.13.2626 · Cited by 205
Goytisolo, F. A., Samper, E., Edmonson, S., Taccioli, G. E., & Blasco, M. A. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.11.3642-3651.2001 · Cited by 199
“well as splenocytes and BM cells from SCID and control wild-type animals, were prepared as described previously (9, 29 , 30).”
MethodInfluentialSelf-citationHarley, C. B. (2002) · Oncogene · doi:10.1038/sj.onc.1205076 · Cited by 194
“Moreover, it has been largely substantiated by the phenotype of the late generation telomerase knockout mouse (Gonzalez-Suarez et al., 2000; Herrera et al., 1999; Lee et al., 1998; Rudolph et al., 1999a), which shares remarkable similarities to the phenotype of the autosomal dominant form of…”
BackgroundPathways connecting telomeres and p53 in senescence, apoptosis, and cancer
Artandi, S. E., & Attardi, L. D. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.03.211 · Cited by 194
Telomeres and Cardiovascular Disease
Serrano, A. L., & Andrés, V. (2004) · Circulation Research · doi:10.1161/01.res.0000122141.18795.9c · Cited by 195
Assessing cell and organ senescence biomarkers
de Jesus, B. B., & Blasco, M. A. (2012) · Circulation Research · doi:10.1161/circresaha.111.247866 · Cited by 187
Self-citationDantzer, F., Giraud-Panis, M.-J. E., Jaco, I., Amé, J., Schultz, I., Blasco, M. A., Koering, C.-E., Gilson, É., Murcia, J. M., de MURCIA, G., et al. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.4.1595-1607.2004 · Cited by 200
“The calibration-corrected telomere fluorescence intensity was calculated as described elsewhere ( 29 ).”
MethodSelf-citationTelomere Shortening in Neural Stem Cells Disrupts Neuronal Differentiation and Neuritogenesis
Ferrón, S. R., Marqués-Torrejón, M. Á., Mira, H., Flores, I., Taylor, K., Blasco, M. A., & Fariñas, I. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.3836-09.2009 · Cited by 179
“…(in mixed C57BL/6/129Sv background), Tercnull mice exhibit a high incidence of critically short telomeres, reduced fertility, and premature aging phenotypes including shorter life span (Blasco et al., 1997; Herrera et al., 1999; Rudolph et al., 1999; Flores et al., 2005; Flores and Blasco, 2009).”
BackgroundSelf-citationAdvances in the understanding of dyskeratosis congenita
Walne, A. J., & Dokal, I. S. (2009) · British Journal of Haematology · doi:10.1111/j.1365-2141.2009.07598.x · Cited by 179
“Many models involving Terc knockout or Tert knockout mice have been generated but these introduce defects that are not seen in the patients as a null in either of these two genes would probably be non-viable in humans (Herrera et al, 1999; Chiang et al, 2004).”
BackgroundBlasco, M. A. (2002) · Nature Reviews Cancer · doi:10.1038/nrc862 · Cited by 175
“Loss of viability owing to short telomeres has also been shown in telomerase-deficient mice, which have premature ageing phenotype”
BackgroundSelf-citationJiang, H., Schiffer, E., Song, Z., Wang, J., Zürbig, P., Thedieck, K., Moes, S., Bantel, H., Saal, N., Jantos, J., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0801457105 · Cited by 169
Telomere Attrition Due to Infection
Ilmonen, P., Kotrschal, A., & Penn, D. J. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002143 · Cited by 174
“capacity of B and T lymphocytes and various diseases [20].”
BackgroundRole of shelterin in cancer and aging
Martínez, P., & Blasco, M. A. (2010) · Aging Cell · doi:10.1111/j.1474-9726.2010.00596.x · Cited by 136
“aplasia, kidney dysfunction, defective bone marrow and proliferative defects of neural stem cells (Lee et al., 1998; Herrera et al., 1999; Samper et al., 2002; Leri et al., 2003; Ferron et al., 2004; Blasco, 2005; Garcia-Cao et al., 2006).”
BackgroundSelf-citationBRCA2 acts as a RAD51 loader to facilitate telomere replication and capping
Badie, S., Escandell, J. M., Bouwman, P., Carlos, A. R., Thanasoula, M., Gallardo, M. M., Suram, A., Jaco, I., Benitez, J. J., Herbig, U., et al. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1943 · Cited by 164
Self-citationSatyanarayana, A., Wiemann, S. U., Buer, J., Lauber, J., Dittmar, K. E. J., Wüstefeld, T., Blasco, M. A., Manns, M. P., & Rudolph, K. L. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg367 · Cited by 158
Self-citationReprogramming of telomerase activity and rebuilding of telomere length in cloned cattle
Betts, D. H., Bordignon, V., Hill, J. R., Winger, Q. A., Westhusin, M. E., Smith, L. C., & King, W. A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.98.3.1077 · Cited by 177
Transformation of normal human cells in the absence of telomerase activation
Seger, Y. R., Garcı́a-Cao, M., Piccinin, S., Cunsolo, C. L., Doglioni, C., Blasco, M. A., Hannon, G. J., & Maestro, R. (2002) · Cancer Cell · doi:10.1016/s1535-6108(02)00183-6 · Cited by 159
“Through genetic analyses, we have also identified require- al., 1998; Herrera et al., 1999, 2000; Samper et al., 2001).”
BackgroundMethodSelf-citationLiu, L., Blasco, M. A., Trimarchi, J. R., & Keefe, D. L. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0735 · Cited by 157
Self-citationTelomeres and telomerase: A dual role in hepatocarcinogenesis
Ande, S., Manns, M. P., & Rudolph, K. L. (2004) · Hepatology · doi:10.1002/hep.20308 · Cited by 166
Aging by epigenetics—A consequence of chromatin damage?
Sedivy, J. M., Gowrishankar, B., & Adams, P. D. (2008) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.02.023 · Cited by 159
“Moreover, manipulation of the cell signals that initiate senescence, such as telomere length and expression of the proliferation inhibitor p16INK4a [66–68,70,73–80], can modulate some aspects of organismal aging [70–72].”
BackgroundPont, A. R., Sadri, N., Hsiao, S. J., Smith, S., & Schneider, R. J. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.04.019 · Cited by 139
“with telomerase knockout mice (Herrera et al., 1999), there was a stronger phenotype and greater decrease in number and survival of Auf1 / offspring in a congenic C57BL/6 background (Figure S2D).”
InfluentialFranceschi, C., Valensin, S., Fagnoni, F., Barbi, C., & Bonafè, M. (1999) · Experimental Gerontology · doi:10.1016/s0531-5565(99)00068-6 · Cited by 154
Ferrón, S., Mira, H., Franco, S., Cano-Jaimez, M., Bellmunt, E., Ramírez, C., Fariñas, I., & Blasco, M. A. (2004) · Development · doi:10.1242/dev.01215 · Cited by 152
“On a mixed C57BL6/129Sv (B6/Sv) genetic background these Terc–/– mice are viable and fertile up to the fifth generation (G5) (Blasco et al., 1997; Lee et al., 1998; Herrera et al., 1999b).”
BackgroundInfluentialSelf-citationBachschmid, M. M., Schildknecht, S., Matsui, R., Zee, R. S., Haeussler, D. J., Cohen, R. A., Pimental, D. R., & van der Loo, B. (2012) · Annals of Medicine · doi:10.3109/07853890.2011.645498 · Cited by 159
Keefe, D. L., Franco, S., Liu, L., Trimarchi, J. R., Cao, B., Weitzen, S. H., Agarwal, S., & Blasco, M. A. (2005) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2005.01.036 · Cited by 143
Self-citationAssociation of telomere length with authentic pluripotency of ES/iPS cells
Huang, J., Wang, F., Okuka, M., Liu, N., Ji, G., Ye, X., Zuo, B., Li, M., Liang, P., Ge, W., et al. (2011) · Cell Research · doi:10.1038/cr.2011.16 · Cited by 148
Mice with bad ends: mouse models for the study of telomeres and telomerase in cancer and aging
Blasco, M. A. (2005) · The EMBO Journal · doi:10.1038/sj.emboj.7600598 · Cited by 152
“…atrophy (Herrera et al, 1999a; Rudolph et al, 1999); (iii) spleen atrophy and reduced proliferation of B and T lymphocytes (Lee et al, 1998; Herrera et al, 1999a); (iv) impaired germinal centre function (Herrera et al, 2000); (v) reduced angiogenic potential (Franco et al, 2002); (vi)…”
BackgroundInfluentialSelf-citationTelomeres and Telomerase in Aging, Regeneration and Cancer
Djojosubroto, M. W., Choi, Y. S., Lee, H., & Rudolph, K. L. (2003) · Molecules and Cells · doi:10.1016/s1016-8478(23)13723-x · Cited by 146
Self-citationImpaired germinal center reaction in mice with short telomeres
Herrera, E., Martínez‐A, C., & Blasco, M. A. (2000) · The EMBO Journal · doi:10.1093/emboj/19.3.472 · Cited by 144
“…on the specific genetic background; however, as telomeres shorten and chromosome fusions accumulate with increasing generations, these mice show defects in the germ line, the gut and the hematopoietic system (Blasco et al., 1997; Lee et al., 1998; Herrera et al., 1999b; Rudolph et al., 1999).”
BackgroundResultInfluentialSelf-citationSchaetzlein, S., Nalapareddy, K., Ju, Z., Lechel, A., Stępczyńska, A., Lilli, D. R., Clark, A. B., Rudolph, C., Kühnel, F., Wei, K., et al. (2007) · Cell · doi:10.1016/j.cell.2007.08.029 · Cited by 146
Tejera, Á. M., d’Alcontres, M. S., Thanasoula, M., Marión, R. M., Martínez, P., Liao, C., Flores, J. M., Tarsounas, M., & Blasco, M. A. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.03.011 · Cited by 157
“Telomere Length and Cytogenetic Analysis Using Telomere Q-FISH on Metaphases Q-FISH onmetaphases from primary MEFswas performed asdescribed (Herrera et al., 1999; Samper et al., 2000). When indicated, MEFs were treated with aphidicolin at 0.5 mM for 24 hr. For analysis of chromosomal aberrations, quantitative analysis…”
MethodInfluentialSelf-citationLong-term repopulating ability of telomerase-deficient murine hematopoietic stem cells
Samper, E., Fernández, P., Eguı́a, R., Martı́n-Rivera, L., Bernad, A., Blasco, M. A., & Aracil, M. (2002) · Blood · doi:10.1182/blood.v99.8.2767 · Cited by 140
Self-citationDefects in telomere maintenance molecules impair osteoblast differentiation and promote osteoporosis
Pignolo, R. J., Suda, R. K., McMillan, E. A., Shen, J., Lee, S., Choi, Y., Wright, A. C., & Johnson, F. B. (2007) · Aging Cell · doi:10.1111/j.1474-9726.2007.00350.x · Cited by 140
Strong, M. A., Vidal-Cardenas, S. L., Karim, B. O., Yu, H. M., Guo, N., & Greider, C. W. (2011) · Molecular and Cellular Biology · doi:10.1128/mcb.05312-11 · Cited by 136
“There was a pronounced decrease in testis size due to germ cell apoptosis (32), and significant degenerative effects were also seen in the hematopoietic system, gastrointestinal (GI) tract, and skin (26, 34, 35, 42, 64, 76).”
BackgroundNiida, H., Shinkai, Y., Hande, M. P., Matsumoto, T., Takehara, S., Tachibana, M., Oshimura, M., Lansdorp, P. M., & Furuichi, Y. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.11.4115-4127.2000 · Cited by 138
“In addition, the much more severe phenotype of mTER C57BL/6 mice (23) compared to mTER mice on a mixed C57BL/6/129 background (33, 48) supports the idea of the genetic background difference.”
BackgroundNF-κB Regulates Transcription of the Mouse Telomerase Catalytic Subunit
Yin, L., Hubbard, A. K., & Giardina, C. A. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m007378200 · Cited by 137
Telomerase abrogation dramatically accelerates TRF2-induced epithelial carcinogenesis
Blanco, R., Muñoz, P., Flores, J. M., Klatt, P., & Blasco, M. A. (2007) · Genes & Development · doi:10.1101/gad.406207 · Cited by 135
“…a normal sensitivity of K5TRF2 cells to -irradiation (Muñoz et al. 2005), and suggest that increased tumorigenesis in G2 and G3 K5TRF2/Terc−/− mice is not likely to be initiated by cancellation of the ATM pathway as a consequence of TRF2 overexpression (Karlseder et al. 2004; Bradshaw et al. 2005).”
BackgroundInfluentialSelf-citationNasir, L., Devlin, P., McKevitt, T. P., Rutteman, G. R., & Argyle, D. J. (2001) · Neoplasia · doi:10.1038/sj.neo.7900173 · Cited by 136
The Retinoblastoma Protein Regulates Pericentric Heterochromatin
Isaac, C. E., Francis, S. M., Martens, A. L., Julian, L. M., Seifried, L. A., Erdmann, N., Binné, U. K., Harrington, L., Sicinski, P., Bérubé, N. G., et al. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.26.9.3659-3671.2006 · Cited by 128
“(25), and centromere fluorescent in situ hybridization”
Cancer and aging: the importance of telomeres in genome maintenance
Rodier, F., Kim, S.-H., Nijjar, T., Yaswen, P., & Campisi, J. (2005) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2004.10.012 · Cited by 132
“For example, telomere shortening and/or dysfunction is evident in certain types of vascular disease, wound healing deficits, and immunosenescence [19-23].”
Background
Metadata
- Authors
- Herrera, E., Samper, E., Martín‐Caballero, J., Flores, J. M., Lee, H., & Blasco, M. A.
- Affiliations
- Consejo Superior de Investigaciones Científicas (ES)
- Universidad Complutense de Madrid (ES)
- Samsung Biomedical Research Institute (KR)
- Corresponding author
- Blasco, María A.
- Venue
- The EMBO Journal
- Published
- 1999-06-01
- Volume
- 18
- Issue
- 11
- Pages
- 2950-2960
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC1171377
- OpenAlex
- W2153094950
- Semantic Scholar
- 2fedd51810926e4acbca1ade7ab5eecd55623631
- Cited by
- 471
- References
- 45
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 8 · 2023: 15 · 2022: 14 · 2021: 13 · 2020: 11 · 2019: 15 · 2018: 15 · 2017: 15 · 2016: 14 · 2015: 9 · 2014: 18 · 2013: 20 · 2012: 20
- FWCI
- 14.72
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The EMBO Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- European Molecular Biology Organization
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Keywords
- telomerase deficiency, telomere shortening, genetic background effects, age-related mortality, fertility, embryonic lethality, neural tube defects, hematopoietic defects, splenic atrophy, hematological abnormalities
- MeSH terms
- Aging, Animals, Atrophy, Body Weight, Cells, Cultured, Crosses, Genetic, Female, Genes, Lethal, Hematopoietic System, Infertility, Intestine, Small, Leukocyte Count, Longevity, Lymphocytes, Male, Mice, Inbred C57BL, Spleen, Testis, Time Factors, Telomere, Mice, Knockout, Telomerase, Mice
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